Economic impact of a peste des petits ruminants outbreak and vaccination cost in northwest Ethiopia

Abstract Peste des petits ruminants (PPR) is an important endemic disease of small ruminants in Ethiopia. While vaccination is widely used in the country to control the disease, quantitative estimates of the actual economic losses due to outbreaks and costs of vaccination are scarce. This study assessed the economic impact and costs of PPR vaccination in Metema district, northwest Ethiopia. The economic impact of the disease was estimated from an outbreak investigation including interviews with 233 smallholder farmers in PPR‐affected kebeles (subdistricts). The cost of PPR vaccination was obtained from vaccination programs in six kebeles of the district and from secondary data in the district veterinary office. In the investigated PPR outbreak, animal‐level PPR morbidity and mortality rates were 51% and 22%, respectively, in sheep and 51% and 25%, respectively, in goats. The flock level morbidity rate was 83% for sheep flocks and 87% for goat flocks. The mean flock level loss was Ethiopian Birr (ETB) 7835 (USD 329 in 2018 average exchange rate) (95% CI: 5954‐9718) for affected sheep flocks and ETB 7136 (USD 300) (95% CI: 5869–8404) for affected goat flocks. The losses in all study flocks during the outbreak were ETB 319 (USD 13.4) per sheep and ETB 306 (USD 12.9) per goat. Mortality accounted for more than 70% of the total losses in both sheep and goat flocks. Vaccination costs for PPR were estimated at ETB 3 per correctly vaccinated animal. Based on the estimated animal‐level direct economic losses and vaccination cost, it can be conjectured that vaccination will pay if a district PPR outbreak occurs more than once every 13 years. This does not account for additional benefits from vaccine‐derived herd immunity reducing disease burden in the wider population. In conclusion, PPR caused high morbidity and mortality in the affected flocks and resulted in high economic losses, equivalent to 14% of annual household income, dramatically affecting the livelihoods of affected flock owners. The vaccination practised in the district is likely to have a positive economic return, with strengthened vaccination programmes bringing reduced economic impact and improved livelihoods.


INTRODUCTION
Peste des petits ruminants (PPR) is an acute or subacute, highly contagious, and economically important transboundary viral disease that imposes a significant constraint upon sheep and goat production in Africa and Asia. It is a frequently fatal disease of sheep and goats caused by the PPR virus (PPRV) of the Morbillivirus genus and Paramyxoviridae family (OIE, 2020). The disease may affect up to 100% of animals in the flock, and an outbreak can kill between 20% and 90% of exposed animals (Albina et al., 2013;Hegde et al., 2009). The disease leads to significant economic, food security, and livelihood impacts in affected communities. In addition to severe production losses associated with mortality and morbidity and costs of control, PPR can also limit trade and prevent the development of intensive small ruminant production .
Ethiopia has a substantial small ruminant population estimated at 31.3 million sheep and 32.7 million goats (Central Statistical Agency [CSA], 2018). Small ruminant production in the country has been burdened with several high-impact transboundary diseases, such as PPR, sheep and goat pox, and contagious caprine pleuropneumonia, with PPR considered a priority livestock disease in Ethiopia (Magona et al., 2016;Waret-Szkuta et al., 2008). For instance, a 5-year (2010−2014) retrospective study revealed a high PPR incidence in the Amhara region (containing 29% of Ethiopian small ruminant population) with 63 reported outbreaks (Fentie et al., 2018).
Vaccination plays a key role in controlling many animal diseases, including PPR, for which a highly effective vaccine is widely used (Roth, 2011;Shimshony & Economides, 2006). It is important to understand the economic justification for any animal health program, including PPR, which is publicly funded in Ethiopia, with many districts conducting vaccination. However, there is a lack of empirical data on the economic impact of the disease and the cost-effectiveness of PPR vaccination. The aim of this study was to estimate the economic impact of PPR outbreaks on smallholder farmers and the costs of vaccination, looking at the case of Metema district in northwest Ethiopia.

Description of the study area and study population
The study was conducted in the Metema district of Amhara Regional State in northwest Ethiopia (Figure 1). Metema district was selected for this study because it has a substantial small ruminant population (152 488 sheep and goats;CSA, 2018), is frequently affected by PPR outbreaks and annual PPR vaccination is practised, albeit with irregular coverage (Yirga et al., 2020). The district has 24 kebeles (subdistricts) and covers an area of approximately 7000 km 2 . The small ruminant flocks have sheep, goats, or both species. The flocks are kept under extensive grazing systems where flocks from different households mix when grazing and at watering points. Sheep and goats in the district F I G U R E 1 Map of the study area showing Metema district, Ethiopia are kept mainly for income generation from the sale of live animals and for home meat consumption but not for milk production (Gizaw et al., 2010

Morbidity and mortality data
During the investigation, to confirm whether a selected flock was affected by PPR during the outbreak, farmers were asked if any disease outbreak had occurred in their flock in the preceding 3 months and if so, they were asked to explain the main epidemiological and clinical features of the outbreak. If the farmer's description matched recognized characteristics of PPR (mucopurulent ocular and/or nasal discharge, oral lesions and/or diarrhoea, which appeared to be contagious affecting several animals in flock), it was considered that PPR had occurred in the flock.
Then, for each production category of sheep and goats, the farmer was asked how many animals were at risk and how many experienced clinical disease, abortion (in case of pregnant animals), or death. PPR treatment costs by group were also ascertained. The animal-level morbidity rate was estimated as the number of animals clinically diseased divided by the total number of animals at risk (considering all sheep and goats in all flocks included in the study), and the flock-level morbidity rate was determined as the number of positive flocks (flocks with one or more animals with clinical PPR) divided by the total number of flocks at risk, that is, all flocks included in the study. The mortality rate was determined as the number of animals that died of PPR during the outbreak divided by the total number of animals at risk.

Mortality loss
Financial loss due to mortality was calculated by considering the five production categories of sheep and goats that died and their corresponding market prices. Price information was collected from four primary markets within the study area by asking the price of 5-10 sheep and goats for each category. All monetary data were collected and calculated using ETB, where 1 ETB was equivalent to USD 0.042 using the 2018 average exchange rate.
Economic loss due to mortality in a flock was calculated as: where ML represents the mortality losses due to PPR in a flock; NADj is the number of animals that died in category j; and Pj is the average price of the animals that died in category j, where j represents the different production categories from j 1 to j 5 .

Body weight loss
Sheep and goats that survive clinical PPR lose weight, and their market value decreases due to this weight loss. The economic loss due to bodyweight loss from PPR was estimated by comparing weights (measured by weight balance) between PPR-affected and nonaffected sheep and goats of similar age and sex in the same flock. When nonaffected animals of similar age and sex were not available in the same flock, animals from a neighbouring flock were used. Four to six pairs of animals were weighed for each category of sheep and goats from all study flocks for this purpose. The difference in weight between affected and unaffected animals was considered the weight loss due to the illness. The economic loss due to body weight loss was estimated as follows: where WL represents the economic loss due to PPR-induced body weight loss in a flock, RAj is the number of PPR recovered animals for category j, BWLj is the average estimated body weight loss for category j, and PL is the average price of live weight/kg.

Abortion loss
The loss due to PPR-induced abortion that was noticed by farmers was estimated. The loss of abortion was difficult to estimate in monetary terms, and the cost of a single aborted fetus was assumed to be half the price of a newborn lamb/kid. Abortion loss was estimated using the following formula: where AL represents the abortion loss in the infected flock, Nabf is the number of foetuses aborted due to PPR in the flock, and Pn is the financial loss from an abortion, which was assumed to be equivalent to 150 ETB (half of the estimated price if new a born lamb/kid).

PPR treatment cost
Treatment cost represents the expense incurred by farmers for the diagnosis and treatment of clinically sick animals at the local public veterinary clinic. The labour cost that farmers incurred for the treatment of sick animals was also included in the treatment cost. Flocklevel treatment cost data were collected by asking farmers. The cost of PPR treatment was calculated as: where TC represents the treatment cost for an affected flock; DMC is diagnosis and medication cost for a flock; NhoursL is the average reported number of working hours the farmer lost from treating sick animals, and Prl is the average price of replacement labour per hour (which was ETB 10/h, derived from the ETB 80 daily wage for unskilled labour).

Overall economic losses
The overall economic loss per individual flock was obtained by adding mortality loss, body weight loss, abortion loss, and treatment cost: where OEL represents the overall economic loss due to PPR per affected flock. Where:

Estimation of the cost of PPR vaccination
Vc represents the vaccine cost; Vp is the vaccine price, which was ETB 0.49/dose, and Sp is the saline price used for reconstituting the vaccine, which was ETB0.04/dose.
Vtc represents the vaccine transport cost after purchase; Tc is the transport truck rental cost; Fc is the fuel cost; and Pc is the cost of transporting personnel.
Fdc represents the field vaccine delivery cost; Cp is the cost of field vaccination personnel (per diem); Tc is the cost of field transport (car rent, fuel, and car maintenance cost); and Mp is the price of materials (consumables).
Cc represents the coordination cost, Cd is the number of coordination days, Pd is per diem, and Tc is the transport cost of the local vaccination coordinator.
Ft represents farmers' time lost during vaccination; Fh represents hours spent by the farmers in getting their flocks vaccinated, and Wh is farmers' wage, which was ETB 10/h.

Outbreak confirmation
Out of 20 samples collected from conjunctival swabs, nasal swabs, and buccal debris of 12 PPR suspected animals, 14 (70%) samples from 8 animals (75%) were positive for PPR viral antigen by Ic-ELISA. The 8 positive animals were found in all four flocks and two kebeles sampled.
Based on this result, the outbreak occurring in the affected kebeles was confirmed to be due to PPRV.

Morbidity and mortality
Of 130 Table 2.
The overall morbidity and mortality rates across the study flocks were 50.7% and 21.6%, respectively, in sheep and 51.3% and 25.1%, respectively, in goats. In the affected flocks, the morbidity and mortality rates were 56% and 24%, respectively, in sheep and 56% and 27%, respectively, in goats. Morbidity and mortality rates were highest in lambs and kids and lowest in adult males in both species.

F I G U R E 3 Components of PPR vaccination costs
in both sheep and goat flocks. Weight loss contributes more to sheep flocks than goat flocks (Figure 2).

Costs of PPR vaccination
The cost per dose of correctly vaccinated animals was estimated to be

DISCUSSION
In this study, we observed a very high household economic impact for flocks affected by PPR (USD 300-329/affected flock approximately 13%-14% annual household income of smallholders in Ethiopia). At the same time, vaccination costs were low (USD 0.13/animal) and could be even lower with less vaccine wastage (> 20% wasted). These findings are relevant to ongoing national and global PPR eradication programs.
The morbidity and mortality rates during the outbreak were 50.7% and 21.6%, respectively, in sheep and 51.3% and 25.1%, respectively, in goats in the study flocks. Morbidity and mortality rates of PPR in the literature are variable depending on several factors, such as the immune status of the population, strain of the virus, species of the animal, etc.
For example, a comparable morbidity rate (53% in sheep and 51% in goats) but a lower mortality rate (13.5% in sheep and 8.5% in goats) was reported from a PPR outbreak in India (Thombare & Sinha, 2009).
However, a much higher average morbidity rate (75%) and mortality rate (59%) were observed in goats from PPR outbreaks in Bangladesh (Chowdhury et al., 2014).
Generally, PPR has a high morbidity rate (90%-100%) and mortality rate (50%-100%), especially in naive populations, but can be lower in endemic situations due to preexisting immunity. This arises from prior vaccination or virus exposure, particularly in older animals, and maternally derived immunity in young stock. Immunity in older animals is reflected in their lower mortality and morbidity in this study (OIE, 2020). Highly variable, but on average lower, morbidity and mortality rates were observed elsewhere in endemic pastoral settings in Africa (Jones et al., 2020). Although there are instances where sheep were more severely affected than goats, goats are considered the most susceptible species for PPR (Kumar et al, 2014). Similar morbidity and mortality rates were observed between sheep and goat flocks in the present study.
Economic evaluation is essential when planning control policy but is seldom done, particularly in low-and middle-income countries, often due to lack of data and lack of familiarity with appropriate methods.
The cost-benefit analysis of the global PPR control program considers only avoided mortality losses (Jones et al., 2016), as estimates of losses from morbidity (without death), although important, are lacking.
In this study, we seek to address this gap by providing estimates of various farm-level PPR impacts and costs and vaccination. We found that mortality accounted for approximately 75%-80% of flock-level losses in the area studied, giving some insight into the underestimated global PPR impact resulting from the exclusion of PPR losses in addition to livestock deaths.  (Kihu et al., 2015).
The second major loss was due to weight loss, which was particularly significant in sheep flocks, accounting for approximately 23% of all economic losses. The contributions of abortion loss, treatment cost, and opportunity cost to farmers' labour were relatively small.
This study only considered short-term direct farm-level impacts, and some estimates were crude (e.g., weight loss and abortion loss).
The impacts of the disease associated with poor growth and reproduction performance are less sudden than mortality but may have large long-term effects on the herd. The impact on trade and milk production (where important) should also not be overlooked.
The present outbreak impact estimates are for an endemic situation where the population had a certain level of immunity, which resulted in lower morbidity and mortality than expected from a PPR outbreak in a naive population. Finally, it is also worth noting that the morbidity and mortality data used for the economic loss estimation were based on farmers' diagnosis of cases in their flocks. Although the outbreak investigated in this study was confirmed to be PPR, it is possible that farmers could miss or misdiagnose cases or conversely have an exaggerated memory of the outbreak, and this will have implications for the accuracy of the loss estimates. Relatedly, mixed flocks, which had larger flock sizes, were excluded from the analysis, as the farmers' recall of the morbidity status of 100 animals in their flock was deemed unreliable.
This exclusion might introduce some undefined bias in the representativeness of the flocks in the study area.
The cost per dose for a vaccinated animal was estimated to be ETB 3.00 (USD 0.13). This was lower than a previous study in Ethiopia that reported ETB 6 for a similar production system .
The difference could be due to larger flock sizes in our study leading to lower per-dose vaccine delivery costs (Tago et al., 2017). Personnel cost was the major component of vaccination cost followed by transport. In a study in Senegal, personnel costs were the major cost component when the number of animals vaccinated per day was small in a smallholder mixed crop-livestock system (Tago et al., 2017). Therefore, careful planning to mobilize smallholders to arrange their animals for vaccination will increase efficiency and reduce the vaccination cost per animal. Furthermore, the estimate of vaccination costs in our study did not include fixed costs, such as the salaries of veterinary personnel and cold chain facilities, which are shared with other veterinary services; the proportion of these costs attributable to PPR control is thought to be too small to significantly affect the estimates and conclusions of this study.
The most effective way to control PPR is a focused area-wide mass immunization of small ruminants, as it is difficult to implement strict sanitary control measures, and stamping out in smallholder systems in countries such as Ethiopia is not feasible. However, the economic efficiency of vaccination needs to be evaluated and optimized. In the present study, although it was not possible to perform a full costbenefit analysis of PPR vaccination, based on the high estimated impact of an outbreak and the low cost of vaccination, PPR vaccination would be expected to deliver positive economic returns.
Considering goats, where the cost per animal in the affected kebele was ETB 306, and 25% of the kebeles in the district were affected, the expected impact per animal in the district would be ETB 76.5 (306 × 0.25), approximately 13 times the cost of giving two doses of vaccination to an animal each year. This suggests that a district-level vaccination break-even point would be if a PPR outbreak would occur once every 13 years without vaccination, which is the case for much of Ethiopia (Fentie et al., 2018). At this point, vaccination becomes costneutral for the district and profitable if outbreaks are more frequent.
Even if outbreaks are less frequent, it may still be advisable to vaccinate regularly to safeguard against the massive short-term economic shock of experiencing an outbreak and its impact on household wellbeing. Furthermore, there are also the long-term population benefits of maintaining high levels of vaccine-derived immunity to reduce virus circulation and disease risk, preventing further spread of PPRV to new areas with progress towards eradication.

CONCLUSIONS
This study identified a high morbidity rate (51% in both sheep and goats) and mortality (22% in sheep and 25% in goats) during a PPR outbreak in small ruminants in Ethiopia. Despite this study not capturing the full impact of the outbreak, we found that affected flocks experienced significant losses, with a mean household loss of USD 329 for sheep and USD 300 for goat flocks, equivalent to on average 14% of annual income for smallholders in these systems, with many more severely affected. Three-quarters of the economic losses were attributed to small ruminant mortality, followed by weight loss in the surviving animals.
A relatively efficient vaccine delivery system resulting from relatively large flock sizes helped keep vaccination costs low (USD 0.13 per dose, including vaccine and delivery costs). Regular vaccination against PPR in the district is likely to be economically profitable at the herd level, with additional benefits at the population level. Vaccination against PPR should be strengthened and expanded. Vaccination delivery should be planned and coordinated with local communities to increase the number of animals vaccinated per day, to maximize coverage, and to minimize vaccine delivery costs.